Elsevier

NeuroImage

Volume 52, Issue 1, 1 August 2010, Pages 245-251
NeuroImage

Functional network interactions during sensorimotor synchronization in musicians and non-musicians

https://doi.org/10.1016/j.neuroimage.2010.03.081Get rights and content

Abstract

Precise timing as determined by sensorimotor synchronization is crucial for a wide variety of activities. Although it is well-established that musicians show superior timing as compared to non-musicians, the neurophysiological foundations – in particular the underlying functional brain network – remain to be characterized. To this end, drummers, professional pianists and non-musicians performed an auditory synchronization task while neuromagnetic activity was measured using a 122-channel whole-head magnetoencephalography (MEG) system. The underlying functional brain network was determined using the beamformer approach Dynamic Imaging of Coherent Sources (DICS). Behaviorally, drummers performed less variably than non-musicians. Neuromagnetic analysis revealed a cerebello-thalamo-cortical network in all subjects comprising bilateral primary sensorimotor cortices (S1/M1), contralateral supplementary motor and premotor regions (SMA and PMC), thalamus, posterior parietal cortex (PPC), ipsilateral cerebellum and bilateral auditory cortices. Stronger PMC–thalamus and PPC–thalamus interactions at alpha and beta frequencies were evident in drummers as compared to non-musicians. In professional pianists stronger PMC–thalamus interaction as compared to non-musicians at beta frequency occurred. The present data suggest that precise timing is associated with increased functional interaction within a PMC–thalamus–PPC network. The PMC–thalamus connectivity at beta frequency might be related to musical expertise, whereas the PPC–thalamus interaction might have specific relevance for precise timing.

Introduction

The temporally precise integration of perception and action becomes most evident in tasks requiring exact timing like musical practice. Experimentally, sensorimotor timing skills can be investigated using a finger tapping task in which finger taps are synchronized with respect to a regularly presented auditory pacing signal. Although subjects have the impression of exact synchrony taps are constantly performed prior to the actual cue. Typically, subjects are not aware of this negative asynchrony (Repp, 2005). Synchronization performance requires the temporally precise integration of multimodal information. The investigation of such presumably transient phenomena requires methods with a high temporal resolution like magnetoencephalography (MEG). Previous studies support the hypothesis that functional interaction – as measured by oscillatory coherence – represents a fundamental mechanism for the integration of information from spatially distributed brain regions (Varela et al., 2001). Along this line, a cerebello-thalamo-cortical network oscillating at 8–12 Hz was shown to be associated with sensorimotor synchronization (Pollok et al., 2005, Pollok et al., 2009).

Interestingly, in finger tapping tasks subjects with musical expertise were shown to have superior synchronization abilities as compared to non-musicians (Repp, 1999, Chen et al., 2006, Chen et al., 2008). Musicians are assumed to use the underlying network more efficiently by activating the same regions to a lesser degree or by recruiting less brain regions for task performance in comparison to non-musicians (Jancke et al., 2000b; Chen et al., 2008). Particularly in musicians, auditory-motor co-activations have been observed indicating functional interaction between auditory and premotor regions (Chen et al., 2006). These findings are in line with the assumption of experience-driven neuroplastic changes and reorganization in musicians (Munte et al., 2002) suggesting an altered functional interplay between brain areas.

However, the neurophysiological origin of superior timing in musicians as compared to non-musicians presently remains elusive. Therefore, this study aims at characterizing (i) the neurophysiological foundations of superior synchronization abilities and (ii) differences in functional network interactions depending on musical expertise. In particular, functional interaction at alpha and beta frequency ranges is focused as both frequency bands have been related to motor control (Schnitzler and Gross, 2005). While beta band coherence is assumed to reflect control of complex movements, alpha band coherence might be associated with automated motor control (Pollok et al., 2009).

Modifications of functional brain interactions have been observed with respect to different task requirements (Pollok et al., 2008, Pollok et al., 2009). Increased subcortical coupling might reflect motor skill learning (Floyer-Lea and Matthews, 2005). Thus, it is reasonable to assume that functional interaction subserving sensorimotor synchronization is modulated by musical training in general and by musical specialization in particular. Therefore, the present study aims at characterizing the functional brain network associated with sensorimotor synchronization in subjects with different musical expertise.

Section snippets

Subjects

Thirty-six healthy subjects participated in the present study. Written informed consent was given prior to the study which was accomplished with the approval of the local ethics committee and is in accordance with the declaration of Helsinki.

All subjects were classified as right-handed by means of the Edinburgh Handedness Inventory (EHI; Oldfield, 1971) and had normal or corrected to normal sight. For right-handedness a minimum EHI score of 60 was required. Professional pianists (6 male, 6

Behavioral data

Analysis of variance (ANOVA) revealed a significant main effect of group (professional pianists vs. drummers vs. non-musicians) for the inter-tap variability of sensorimotor synchronization (F(2, 35) = 10.32, p < .001; Fig. 1). Post hoc Scheffé test showed a significantly lower inter-tap variability in drummers as compared to non-musicians (p < .001). Inter-tap variability neither significantly differed between professional pianists and drummers (p = .078) nor between professional pianists and

Discussion

The present study aimed at investigating the effect of musical expertise and musical specialization on functional network interactions associated with accurate timing in the sub-second range. To this end, the functional brain network subserving sensorimotor synchronization was investigated in drummers, professional pianists and non-musicians. Drummers performed less variably and, thus, superior as compared to the non-musicians. This observation is in line with superior timing skills evidenced

Acknowledgments

Bettina Pollok is grateful for financial support by a grant from Heinrich-Heine-University (9772328). Alfons Schnitzler is supported by the VolkswagenStiftung (I/80191). We thank Erika Rädisch for technical support with MRI data acquisition.

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